The arabidopsis GRAS protein SCL14 interacts with class II TGA transcription factors and is essential for the activation of stress-inducible promoters

Plant Cell

Volumn 20, Issue 11, 2008, Pages 3122-3135

  Fode, Benjamin ^a   Siemsen, Tanja ^a   Thurow, Corinna ^a   Weigel, Ralf ^a   Gatz, Christiane ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 58549104358     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.108.058974     Document Type: Article

References (70)

1. Apel, K., and Hirt, H. (2004). Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55: 373-399.
2. Baerson, S.R., Sanchez-Moreiras, A., Pedrol-Bonjoch, N., Schulz, M., Kagan, I.A., Agarwal, A.K., Reigosa, M.J., and Duke, S.O. (2005). Detoxification and transcriptome response in Arabidopsis seedlings exposed to the allelochemical benzoxazolin-2(3H)-one. J. Biol. Chem. 280: 21867-21881.
3. Bensmihen, S., To, A., Lambert, G., Kroj, T., Giraudat, J., and Parcy, F. (2004). Analysis of an activated ABI5 allele using a new selection method for transgenic Arabidopsis seeds. FEBS Lett. 561: 127-131.
4. Blanco, F., Garreton, V., Frey, N., Dominguez, C., Perez-Acle, T., Van der Straeten, D., Jordana, X., and Holuigue, L. (2005). Identification of NPR1-dependent and independent genes early induced by salicylic acid treatment in Arabidopsis. Plant Mol. Biol. 59: 927-944.
5. Bolle, C. (2004). The role of GRAS proteins in plant signal transduction and development. Planta 218: 683-692.
6. Bretz, F., Landgrebe, J., and Brunner, E. (2005). Multiplicity issues in microarray experiments. Methods Inf. Med. 44: 431-437.
7. Butterbrodt, T., Thurow, C., and Gatz, C. (2006). Chromatin immuno- precipitation analysis of the tobacco PR-1a- and the truncated CaMV 35S promoter reveals differences in salicylic acid-dependent TGA factor binding and histone acetylation. Plant Mol. Biol. 61: 665-674.
8. Cao, H., Glazebrook, J., Clarke, J.D., Volko, S., and Dong, X. (1997). The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88: 57-63.
9. Chen, W., and Singh, K.B. (1999). The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element. Plant J. 19: 667-677.
10. Chiu, W., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H., and Sheen, J. (1996). Engineered GFP as a vital reporter in plants. Curr. Biol. 6: 325-330.
11. Chomczynski, P., and Mackey, K. (1995). Short technical reports. Modification of the TRI reagent procedure for isolation of RNA from polysaccharide- and proteoglycan-rich sources. Biotechniques 19: 942-945.
12. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium- mediated transformation of Arabodopsis thaliana. Plant J. 16: 735-743.
13. Czechowski, T., Stitt, M., Altmann, T., Udvardi, M.K., and Scheible, W.R. (2005). Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 139: 5-17.
14. Denison, M.S., and Nagy, S.R. (2003). Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu. Rev. Pharmacol. Toxicol. 43: 309-334.
15. Di Laurenzio, L., Wysocka-Diller, J., Malamy, J.E., Pysh, L., Helariutta, Y., Freshour, G., Hahn, M.G., Feldmann, K.A., and Benfey, P.N. (1996). The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 86: 423-433.
16. Dill, A., Thomas, S.G., Hu, J., Steber, C.M., and Sun, T.P. (2004). The Arabidopsis F-box protein SLEEPY1 targets gibberellin signaling repressors for gibberellin-induced degradation. Plant Cell 16: 1392-1405.
17. Ekman, D.R., Lorenz, W.W., Przybyla, A.E., Wolfe, N.L., and Dean, J. F. (2003). SAGE analysis of transcriptome responses in Arabidopsis roots exposed to 2,4,6-trinitrotoluene. Plant Physiol. 133: 1397-1406.
18. Fan, W., and Dong, X. (2002). In vivo interaction between NPR1 and transcription factor TGA2 leads to salicylic acid-mediated gene activation in Arabidopsis. Plant Cell 14: 1377-1389.
19. Fields, S., and Song, O. (1989). A novel genetic system to detect protein-protein interactions. Nature 340: 245-246.
20. Fobert, P.R., and Despres, C. (2005). Redox control of systemic acquired resistance. Curr. Opin. Plant Biol. 8: 378-382.
21. Gao, M.J., Parkin, I., Lydiate, D., and Hannoufa, A. (2004). An auxin- responsive SCARECROW-like transcriptional activator interacts with histone deacetylase. Plant Mol. Biol. 55: 417-431.
22. Gietz, R.D., Schiestl, R.H., Willems, A.R., and Woods, R.A. (1995). Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast 11: 355-360.
23. Haasen, D., Kohler, C., Neuhaus, G., and Merkle, T. (1999). Nuclear export of proteins in plants: AtXPO1 is the export receptor for leucine- rich nuclear export signals in Arabidopsis thaliana. Plant J. 20: 695-705.
24. Heinekamp, T., Kuhlmann, M., Lenk, A., Strathmann, A., and Droge-Laser, W. (2002). The tobacco bZIP transcription factor BZI-1 binds to G-box elements in the promoters of phenylpropanoid pathway genes in vitro, but it is not involved in their regulation in vivo. Mol. Genet. Genomics 267: 16-26.
25. James, P., Halladay, J., and Craig, E.A. (1996). Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144: 1425-1436.
26. Johnson, C., Boden, E., and Arias, J. (2003). Salicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis. Plant Cell 15: 1846-1858.
27. Katagiri, F., Lam, E., and Chua, N.H. (1989). Two tobacco DNA- binding proteins with homology to the nuclear factor CREB. Nature 340: 727-730.
28. Katzer, M. (2004). Automatic Segmentation of Microarray Images. PhD dissertation (Bielefeld, Germany: Universität Bielefeld).
29. Kholod, N., and Mustelin, T. (2001). Novel vectors for co-expression of two proteins in E. coli. Biotechniques 31: 322-323, 326-328.
30. Kliewer, S.A., Goodwin, B., and Willson, T.M. (2002). The nuclear pregnane X receptor: A key regulator of xenobiotic metabolism. Endocr. Rev. 23: 687-702.
31. Klinedinst, S., Pascuzzi, P., Redman, J., Desai, M., and Arias, J. (2000). A xenobiotic-stress-activated transcription factor and its cognate target genes are preferentially expressed in root tip meristems. Plant Mol. Biol. 42: 679-688.
32. Krawczyk, S., Thurow, C., Niggeweg, R., and Gatz, C. (2002). Analysis of the spacing between the two palindromes of activation sequence-1 with respect to binding to different TGA factors and transcriptional activation potential. Nucleic Acids Res. 30: 775-781.
33. Kudo, N., Matsumori, N., Taoka, H., Fujiwara, D., Schreiner, E.P., Wolff, B., Yoshida, M., and Horinouchi, S. (1999). Leptomycin B inactivates CRM1/exportin 1 by covalent modification at a cysteine residue in the central conserved region. Proc. Natl. Acad. Sci. USA 96: 9112-9117.
34. Kyhse- Andersen, J. (1984). Electroblotting of multiple gels: A simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J. Biochem. Biophys. Methods 10: 203-209.
35. Lam, E., Benfey, P.N., Gilmartin, P.M., Fang, R.X., and Chua, N.H. (1989). Site-specific mutations alter in vitro factor binding and change promoter expression pattern in transgenic plants. Proc. Natl. Acad. Sci. USA 86: 7890-7894.
36. Lebel, E., Heifetz, P., Thorne, L., Uknes, S., Ryals, J., and Ward, E. (1998). Functional analysis of regulatory sequences controlling PR-1 gene expression in Arabidopsis. Plant J. 16: 223-233.
37. Li, X., Zhang, Y., Clarke, J.D., Li, Y., and Dong, X. (1999). Identification and cloning of a negative regulator of systemic acquired resistance, SNI1, through a screen for suppressors of npr1-1. Cell 98: 329-339.
38. Liu, X., and Lam, E. (1994). Two binding sites for the plant transcription factor ASF-1 can respond to auxin treatments in transgenic tobacco. J. Biol. Chem. 269: 668-675.
39. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)).Methods 25: 402-408.
40. Minet, M., Dufour, M.E., and Lacroute, F. (1992). Complementation of Saccharomyces cerevisiae auxotrophic mutants by Arabidopsis thaliana cDNAs. Plant J. 2: 417-422.
41. Morohashi, K., Minami, M., Takase, H., Hotta, Y., and Hiratsuka, K. (2003). Isolation and characterization of a novel GRAS gene that regulates meiosis-associated gene expression. J. Biol. Chem. 278: 20865-20873.
42. Mou, Z., Fan, W., and Dong, X. (2003). Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes. Cell 113: 935-944.
43. Muckenschnabel, I., Goodman, B.A., Williamson, B., Lyon, G.D., and Deighton, N. (2002). Infection of leaves of Arabidopsis thaliana by Botrytis cinerea: Changes in ascorbic acid, free radicals and lipid peroxidation products. J. Exp. Bot. 53: 207-214.
44. Mueller, S., Hilbert, B., Dueckershoff, K., Roitsch, T., Krischke, M., Mueller, M.J., and Berger, S. (2008). General detoxification and stress responses are mediated by oxidized lipids through TGA transcription factors in Arabidopsis. Plant Cell 20: 768-785.
45. Ndamukong, I., Al Abdallat, A., Thurow, C., Fode, B., Zander, M., Weigel, R., and Gatz, C. (2007). SA-inducible Arabidopsis glutare- doxin interacts with TGA factors and suppresses JA-responsive PDF1.2 transcription. Plant J. 50: 128-139.
46. Nguyen, T., Sherratt, P.J., and Pickett, C.B. (2003). Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. Annu. Rev. Pharmacol. Toxicol. 43: 233-260.
47. Niggeweg, R., Thurow, C., Weigel, R., Pfitzner, U., and Gatz, C. (2000). Tobacco TGA factors differ with respect to interaction with NPR1, activation potential and DNA-binding properties. Plant Mol. Biol. 42: 775-788.
48. Pascuzzi, P., Hamilton, D., Bodily, K., and Arias, J. (1998). Auxininduced stress potentiates trans-activation by a conserved plant basic/leucine-zipper factor. J. Biol. Chem. 273: 26631-26637.
49. Prelic, A., Bleuler, S., Zimmermann, P., Wille, A., Bühlmann, P., Gruissem, W., Hennig, L., Thiele, L., and Zitzler, E. (2006). Comparison of biclustering methods: A systematic comparison and evaluation of biclustering methods for gene expression data. Bioinformatics 22: 1122-1129.
50. Pysh, L.D., Wysocka-Diller, J.W., Camilleri, C., Bouchez, D., and Benfey, P.N. (1999). The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J. 18: 111-119.
51. Qin, X.F., Holuigue, L., Horvath, D.M., and Chua, N.H. (1994). Immediate early transcription activation by salicylic acid via the cauliflower mosaic virus as-1 element. Plant Cell 6: 863-874.
52. Redman, J., Whitcraft, J., Gulam, H., and Arias, J. (2002). Abiotic and biotic stress differentially stimulate as-1 element activity in Arabidop- sis. Plant Cell Rep. 21: 180-185.
53. Riechmann, J.L., et al. (2000). Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290: 2105-2110.
54. Rochon, A., Boyle, P., Wignes, T., Fobert, P.R., and Despres, C. (2006). The coactivator function of Arabidopsis NPR1 requires the core of Its BTB/POZ domain and the oxidation of C-terminal cysteines. Plant Cell 18: 3670-3685.
55. Ryals, J., Weymann, K., Lawton, K., Friedrich, L., Ellis, D., Steiner, H. Y., Johnson, J., Delaney, T.P., Jesse, T., Vos, P., and Uknes, S. (1997). The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B. Plant Cell 9: 425-439.
56. Sandermann, H., Jr. (1992). Plant metabolism of xenobiotics. Trends Biochem. Sci. 17: 82-84.
57. Schiermeyer, A., Thurow, C., and Gatz, C. (2003). Tobacco bZIP factor TGA10 is a novel member of the TGA family of transcription factors. Plant Mol. Biol. 51: 817-829.
58. Siemering, K.R., Golbik, R., Sever, R., and Haseloff, J. (1996). Mutations that suppress the thermosensitivity of green fluorescent protein. Curr. Biol. 6: 1653-1663.
59. Silverstone, A.L., Ciampaglio, C.N., and Sun, T. (1998). The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10: 155-169.
60. Thurow, C., Schiermeyer, A., Krawczyk, S., Butterbrodt, T., Nickolov, K., and Gatz, C. (2005). Tobacco bZIP transcription factor TGA2.2 and related factor TGA2.1 have distinct roles in plant defense responses and plant development. Plant J. 44: 100-113.
61. Tian, C., Wan, P., Sun, S., Li, J., and Chen, M. (2004). Genome-wide analysis of the GRAS gene family in rice and Arabidopsis. Plant Mol. Biol. 54: 519-532.
62. Torres, M.A., Jones, J.D.G., and Dangl, J.L. (2005). Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat. Genet. 37: 1130-1134.
63. Uquillas, C., Letelier, I., Blanco, F., Jordana, X., and Holuigue, L. (2004). NPR1-independent activation of immediate early salicylic acid-responsive genes in Arabidopsis. Mol. Plant Microbe Interact. 17: 34-42.
64. Wagner, U., Edwards, R., Dixon, D.P., and Mauch, F. (2002). Probing the diversity of the Arabidopsis glutathione S-transferase gene family. Plant Mol. Biol. 49: 515-532.
65. Weigel, R.R., Bauscher, C., Pfitzner, A.J., and Pfitzner, U.M. (2001). NIMIN-1, NIMIN-2 and NIMIN-3, members of a novel family of proteins from Arabidopsis that interact with NPR1/NIM1, a key regulator of systemic acquired resistance in plants. Plant Mol. Biol. 46: 143-160.
66. Weigel, R.R., Pfitzner, U.M., and Gatz, C. (2005). Interaction of NIMIN1 with NPR1 modulates PR gene expression in Arabidopsis. Plant Cell 17: 1279-1291.
67. Zentella, R., Zhang, Z.L., Park, M., Thomas, S.G., Endo, A., Murase, K., Fleet, C.M., Jikumaru, Y., Nambara, E., Kamiya, Y., and Sun, T. P. (2007). Global analysis of della direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19: 3037-3057.
68. Zhang, B., and Singh, K.B. (1994). ocs element promoter sequences are activated by auxin and salicylic acid in Arabidopsis. Proc. Natl. Acad. Sci. USA 91: 2507-2511.
69. Zhang, Y.L., Tessaro, M.J., Lassner, M., and Li, X. (2003). Knockout analysis of Arabidopsis transcription factors TGA2, TGA5, and TGA6 reveals their redundant and essential roles in systemic acquired resistance. Plant Cell 15: 2647-2653.
70. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and Gruissem, W. (2004). GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136: 2621-2632.